MiR-30a attenuates immunosuppressive functions of IL-1β-elicited mesenchymal stem cells via targeting TAB3

FEBS Letters

Volumn 589, Issue 24, 2015, Pages 3899-3907

  Hu, Erling ^a   Ding, Liang ^a   Miao, Huishuang ^a   Liu, Fei ^a   Liu, Dan ^a   Dou, Huan ^a   Hou, Yayi ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

Immunoregulatory function; Interleukin 1 ; Mesenchymal stem cell; MiR 30a; TAK1 binding protein 3

Indexed keywords

BINDING PROTEIN; CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MICRORNA; MICRORNA 30A; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1 BINDING PROTEIN 3; UNCLASSIFIED DRUG; LIPOPOLYSACCHARIDE; MIRN30 MICRORNA, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; PTGS2 PROTEIN, HUMAN; SIGNAL PEPTIDE; TAB3 PROTEIN, HUMAN;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL FUNCTION; CYTOKINE PRODUCTION; ENZYME INHIBITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREGULATION; MACROPHAGE; MESENCHYMAL STEM CELL; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UMBILICAL CORD COMPLICATION; BIOSYNTHESIS; CELL CYCLE; CYTOLOGY; DRUG EFFECTS; FEMALE; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; PREGNANCY; UMBILICAL CORD; UPREGULATION;

BASE SEQUENCE; CELL CYCLE; CYCLOOXYGENASE 2; FEMALE; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKIN-8; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPOLYSACCHARIDES; MACROPHAGES; MAP KINASE KINASE 4; MESENCHYMAL STROMAL CELLS; MICRORNAS; NF-KAPPA B; PRE-ECLAMPSIA; PREGNANCY; SIGNAL TRANSDUCTION; UMBILICAL CORD; UP-REGULATION;

EID: 84959498318     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.11.001     Document Type: Article

References (61)

1. L.T. Medeiros, Monocytes from pregnant women with pre-eclampsia are polarized to a M1 phenotype. Am. J. Reprod. Immunol., 72, (2014), 5-13.
2. S. Venkatesha, Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat. Med., 12, (2006), 642-649.
3. K. Kanasaki, R. Kalluri, The biology of preeclampsia. Kidney Int., 76, (2009), 831-837.
4. E. Laresgoiti-Servitje, A leading role for the immune system in the pathophysiology of preeclampsia. J. Leukoc. Biol., 94, (2013), 247-257.
5. A. Dorronsoro, J. Fernandez-Rueda, K. Fechter, I. Ferrin, J.M. Salcedo, E. Jakobsson, C. Trigueros, Human mesenchymal stromal cell-mediated immunoregulation: mechanisms of action and clinical applications. Bone Marrow Res., 2013, (2013), 203643 -
6. M. Gazdic, V. Volarevic, N. Arsenijevic, M. Stojkovic, Mesenchymal stem cells: a friend or foe in immune-mediated diseases. Stem Cell Rev., (2015)
7. Y. Jiang, Pluripotency of mesenchymal stem cells derived from adult marrow. Nature, 418, (2002), 41-49.
8. M. Dominici, Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8, (2006), 315-317.
9. L. Liu, MicroRNA-181a regulates local immune balance by inhibiting proliferation and immunosuppressive properties of mesenchymal stem cells. Stem Cells, 30, (2012), 1756-1770.
10. I. Rasmusson, K. Le Blanc, B. Sundberg, O. Ringden, Mesenchymal stem cells stimulate antibody secretion in human B cells. Scand. J. Immunol., 65, (2007), 336-343.
11. Y. Deng, Umbilical cord-derived mesenchymal stem cells instruct dendritic cells to acquire tolerogenic phenotypes through the IL-6-mediated upregulation of SOCS1. Stem Cells Dev., 23, (2014), 2080-2092.
12. X. Zhao, D. Liu, W. Gong, G. Zhao, L. Liu, L. Yang, Y. Hou, The toll-like receptor 3 ligand, poly(I:C), improves immunosuppressive function and therapeutic effect of mesenchymal stem cells on sepsis via inhibiting MiR-143. Stem Cells, 32, (2014), 521-533.
13. S.J. Prasanna, D. Gopalakrishnan, S.R. Shankar, A.B. Vasandan, Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PLoS ONE, 5, (2010), e9016 -
14. M. Krampera, Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells, 24, (2006), 386-398.
15. E. Lombardo, T. van der Poll, O. DelaRosa, W. Dalemans, Mesenchymal stem cells as a therapeutic tool to treat sepsis. World J. Stem Cells, 7, (2015), 368-379.
16. A. Rolfo, D. Giuffrida, A.M. Nuzzo, D. Pierobon, S. Cardaropoli, E. Piccoli, M. Giovarelli, T. Todros, Pro-inflammatory profile of preeclamptic placental mesenchymal stromal cells: new insights into the etiopathogenesis of preeclampsia. PLoS ONE, 8, (2013), e59403 -
17. D.P. Bartel, MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, (2004), 281-297.
18. A. Zampetaki, M. Mayr, MicroRNAs in vascular and metabolic disease. Circ. Res., 110, (2012), 508-522.
19. Y. Luo, Increased serum and urinary microRNAs in children with idiopathic nephrotic syndrome. Clin. Chem., 59, (2013), 658-666.
20. L. Anton, A.O. Olarerin-George, J.B. Hogenesch, M.A. Elovitz, Placental expression of miR-517a/b and miR-517c contributes to trophoblast dysfunction and preeclampsia. PLoS ONE, 10, (2015), e0122707 -
21. L. Anton, A.O. Olarerin-George, N. Schwartz, S. Srinivas, J. Bastek, J.B. Hogenesch, M.A. Elovitz, MiR-210 inhibits trophoblast invasion and is a serum biomarker for preeclampsia. Am. J. Pathol., 183, (2013), 1437-1445.
22. Y. Zhang, Z. Diao, L. Su, H. Sun, R. Li, H. Cui, Y. Hu, MicroRNA-155 contributes to preeclampsia by down-regulating CYR61. Am. J. Obstet. Gynecol., 202, 466 (2010), e1-e7.
23. Q. Li, Z. Pan, X. Wang, Z. Gao, C. Ren, W. Yang, MiR-125b-1-3p inhibits trophoblast cell invasion by targeting sphingosine-1-phosphate receptor 1 in preeclampsia. Biochem. Biophys. Res. Commun., 453, (2014), 57-63.
24. Y. Bai, Downregulated miR-195 detected in preeclamptic placenta affects trophoblast cell invasion via modulating ActRIIA expression. PLoS ONE, 7, (2012), e38875 -
25. Y. Wang, H. Fan, G. Zhao, D. Liu, L. Du, Z. Wang, Y. Hu, Y. Hou, MiR-16 inhibits the proliferation and angiogenesis-regulating potential of mesenchymal stem cells in severe pre-eclampsia. FEBS J., 279, (2012), 4510-4524.
26. S. Chen, G. Zhao, H. Miao, R. Tang, Y. Song, Y. Hu, Z. Wang, Y. Hou, MicroRNA-494 inhibits the growth and angiogenesis-regulating potential of mesenchymal stem cells. FEBS Lett., 589, (2015), 710-717.
27. N. Zhang, X. Wang, Q. Huo, M. Sun, C. Cai, Z. Liu, G. Hu, Q. Yang, MicroRNA-30a suppresses breast tumor growth and metastasis by targeting metadherin. Oncogene, 33, (2014), 3119-3128.
28. J. Fu, MiR-30a suppresses breast cancer cell proliferation and migration by targeting Eya2. Biochem. Biophys. Res. Commun., 445, (2014), 314-319.
29. T. Ichimi, Identification of novel microRNA targets based on microRNA signatures in bladder cancer. Int. J. Cancer, 125, (2009), 345-352.
30. R. Baffa, MicroRNA expression profiling of human metastatic cancers identifies cancer gene targets. J. Pathol., 219, (2009), 214-221.
31. T. Eguchi, K. Watanabe, E.S. Hara, M. Ono, T. Kuboki, S.K. Calderwood, OstemiR: a novel panel of microRNA biomarkers in osteoblastic and osteocytic differentiation from mesenchymal stem cells. PLoS ONE, 8, (2013), e58796 -
32. L. Cui, A set of microRNAs mediate direct conversion of human umbilical cord lining-derived mesenchymal stem cells into hepatocytes. Cell Death Dis., 4, (2013), e918 -
33. L. Du, H. Fan, H. Miao, G. Zhao, Y. Hou, Extremely low frequency magnetic fields inhibit adipogenesis of human mesenchymal stem cells. Bioelectromagnetics, 35, (2014), 519-530.
34. H. Fan, Pre-treatment with IL-1beta enhances the efficacy of MSC transplantation in DSS-induced colitis. Cell. Mol. Immunol., 9, (2012), 473-481.
35. D.J. Barbeau, K.T. La, D.S. Kim, S.S. Kerpedjieva, G.V. Shurin, K. Tamama, Early growth response-2 signaling mediates immunomodulatory effects of human multipotential stromal cells. Stem Cells Dev., 23, (2014), 155-166.
36. J.E. Siljee, Identification of interleukin-1 beta, but no other inflammatory proteins, as an early onset pre-eclampsia biomarker in first trimester serum by bead-based multiplexed immunoassays. Prenat. Diagn., 33, (2013), 1183-1188.
37. M. Kalinderis, A. Papanikolaou, K. Kalinderi, E. Ioannidou, C. Giannoulis, V. Karagiannis, B.C. Tarlatzis, Elevated serum levels of interleukin-6, interleukin-1beta and human chorionic gonadotropin in pre-eclampsia. Am. J. Reprod. Immunol., 66, (2011), 468-475.
38. T. Nagamatsu, D.J. Schust, The immunomodulatory roles of macrophages at the maternal-fetal interface. Reprod. Sci., 17, (2010), 209-218.
39. P.C. Cheung, A.R. Nebreda, P. Cohen, TAB3, a new binding partner of the protein kinase TAK1. Biochem. J., 378, (2004), 27-34.
40. X. Lei, N. Han, X. Xiao, Q. Jin, B. He, J. Wang, Enterovirus 71 3C inhibits cytokine expression through cleavage of the TAK1/TAB1/TAB2/TAB3 complex. J. Virol., 88, (2014), 9830-9841.
41. J.H. Hwang, M.J. Lee, O.S. Seok, Y.C. Paek, G.J. Cho, H.J. Seol, J.K. Lee, M.J. Oh, Cytokine expression in placenta-derived mesenchymal stem cells in patients with pre-eclampsia and normal pregnancies. Cytokine, 49, (2010), 95-101.
42. S. Muralimanoharan, A. Maloyan, J. Mele, C. Guo, L.G. Myatt, L. Myatt, MIR-210 modulates mitochondrial respiration in placenta with preeclampsia. Placenta, 33, (2012), 816-823.
43. Y. Zhang, N. Matsushita, T. Eigler, E. Marban, Targeted microRNA interference promotes postnatal cardiac cell cycle re-entry. J. Regen. Med., 2, (2013), 2 -
44. A. Amash, G. Holcberg, O. Sapir, M. Huleihel, Placental secretion of interleukin-1 and interleukin-1 receptor antagonist in preeclampsia: effect of magnesium sulfate. J. Interferon Cytokine Res., 32, (2012), 432-441.
45. S.A. Jones, Directing transition from innate to acquired immunity: defining a role for IL-6. J. Immunol., 175, (2005), 3463-3468.
46. M.R. Fernando, J.L. Reyes, J. Iannuzzi, G. Leung, D.M. McKay, The pro-inflammatory cytokine, interleukin-6, enhances the polarization of alternatively activated macrophages. PLoS ONE, 9, (2014), e94188 -
47. H. Roca, Z.S. Varsos, S. Sud, M.J. Craig, C. Ying, K.J. Pienta, CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J. Biol. Chem., 284, (2009), 34342-34354.
48. P. Li, S.H. Li, J. Wu, W.F. Zang, S. Dhingra, L. Sun, R.D. Weisel, R.K. Li, Interleukin-6 downregulation with mesenchymal stem cell differentiation results in loss of immunoprivilege. J. Cell. Mol. Med., 17, (2013), 1136-1145.
49. F. Djouad, Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependent mechanism. Stem Cells, 25, (2007), 2025-2032.
50. X.X. Jiang, Y. Zhang, B. Liu, S.X. Zhang, Y. Wu, X.D. Yu, N. Mao, Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood, 105, (2005), 4120-4126.
51. A.J. Nauta, A.B. Kruisselbrink, E. Lurvink, R. Willemze, W.E. Fibbe, Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J. Immunol., 177, (2006), 2080-2087.
52. S. Aggarwal, M.F. Pittenger, Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood, 105, (2005), 1815-1822.
53. C. Trento, F. Dazzi, Mesenchymal stem cells and innate tolerance: biology and clinical applications. Swiss Med. Wkly., 140, (2010), w13121 -
54. K. Nemeth, Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat. Med., 15, (2009), 42-49.
55. E. Eggenhofer, M.J. Hoogduijn, Mesenchymal stem cell-educated macrophages. Transplant. Res., 1, (2012), 12 -
56. M.M. Faas, F. Spaans, P. De Vos, Monocytes and macrophages in pregnancy and pre-eclampsia. Front. Immunol., 5, (2014), 298 -
57. A. Kanayama, TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol. Cell, 15, (2004), 535-548.
58. X. Liu, IL-1beta induces IL-6 production in retinal Muller cells predominantly through the activation of p38 MAPK/NF-kappaB signaling pathway. Exp. Cell Res., 331, (2015), 223-231.
59. T. Ishitani, G. Takaesu, J. Ninomiya-Tsuji, H. Shibuya, R.B. Gaynor, K. Matsumoto, Role of the TAB2-related protein TAB3 in IL-1 and TNF signaling. EMBO J., 22, (2003), 6277-6288.
60. A. Besse, B. Lamothe, A.D. Campos, W.K. Webster, U. Maddineni, S.C. Lin, H. Wu, B.G. Darnay, TAK1-dependent signaling requires functional interaction with TAB2/TAB3. J. Biol. Chem., 282, (2007), 3918-3928.
61. Y.S. Roh, J. Song, E. Seki, TAK1 regulates hepatic cell survival and carcinogenesis. J. Gastroenterol., 49, (2014), 185-194.